Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus

Plant Journal

Volumn 62, Issue 4, 2010, Pages 674-688

  Mohamed, Rozi ^a,d   Wang, Chieh Ting ^b,e   Ma, Cathleen ^a   Shevchenko, Olga ^a   Dye, Sarah J ^a   Puzey, Joshua R ^b,f   Etherington, Elizabeth ^a   Sheng, Xiaoyan ^b   Meilan, Richard ^c   Strauss, Steven H ^a   Brunner, Amy M ^b  

^a OREGON STATE UNIVERSITY   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c PURDUE UNIVERSITY   (United States)

^d UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

^f HARVARD UNIVERSITY   (United States)

Author keywords

Axillary meristem; Branching; Dormancy; Flowering; Populus; TERMINAL FLOWER 1

Indexed keywords

AGE-RELATED CHANGES; AXILLARY MERISTEM; CONTROLLED ENVIRONMENT; DOWN-REGULATION; FIELD STUDIES; HERBACEOUS PLANTS; IN-PLANTS; MATURE TREES; MERISTEM IDENTITY; ORTHOLOGS; OVER-EXPRESSION; PARALOGS; POPULUS; POPULUS SPP; RNA INTERFERENCE; SEASONAL CYCLE; SHOOT APEX; SHOOT SYSTEMS; SHORT SHOOTS; TRANSGENIC POPLARS; TRANSGENICS; WILD TYPES; WOODY PERENNIALS;

FORESTRY; RNA;

PLANTS (BOTANY);

PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; ASPEN; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INFLORESCENCE; MERISTEM; METABOLISM; RNA INTERFERENCE; TRANSGENIC PLANT;

GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; INFLORESCENCE; MERISTEM; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POPULUS; RNA INTERFERENCE; RNA, PLANT; SEQUENCE ANALYSIS, DNA;

FORESTRY; NUCLEIC ACIDS; PLANTS; POPULUS;

POPULUS;

EID: 77952175312     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04185.x     Document Type: Article

References (70)

1. Ahn, J.H., Miller, D., Winter, V.J., Banfield, M.J., Lee, J.H., Yoo, S.Y., Henz, S.R., Brady, R.L. Weigel, D. (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J. 25, 605 614.
2. Boes, T.K. Strauss, S.H. (1994) Floral phenology and morphology of black cottonwood, Populus trichocarpa (Salicaceae). Am. J. Bot. 81, 562 567.
3. Bohlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A.M., Jansson, S., Strauss, S.H. Nilsson, O. (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science, 312, 1040 1043.
4. Bradley, D., Carpenter, R., Copsey, L., Vincent, C., Rothstein, S. Coen, E. (1996) Control of inflorescence architecture in Antirrhinum. Nature, 379, 791 797.
5. Bradley, D., Ratcliffe, O., Vincent, C., Carpenter, R. Coen, E. (1997) Inflorescence commitment and architecture in Arabidopsis. Science, 275, 80 83.
6. Brunner, A.M. Nilsson, O. (2004) Revisiting tree maturation and floral initiation in the poplar functional genomics era. New Phytol. 164, 43 51.
7. Brunner, A.M., Goldfarb, B., Busov, V. Strauss, S.H. (2003) Controlling maturation and flowering for forest tree domestication. In Transgenic Plants: Current Innovations and Future Trends (Stewart, C.N. ed
8. Brunner, A.M., Yakovlev, I.A. Strauss, S.H. (2004) Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol. 4, 14.
9. Brunner, A., Li, J., DiFazio, S. et al. (2007) Genetic containment of forest plantations. Tree Genet. Genomes, 3, 75 100.
10. Conti, L. Bradley, D. (2007) TERMINAL FLOWER1 is a mobile signal controlling Arabidopsis architecture. Plant Cell, 19, 767 778.
11. Critchfield, W.B. (1960) Leaf dimorphism in Populus trichocarpa. Am. J. Bot. 47, 69 711.
12. Danilevskaya, O.N., Meng, X., Hou, Z., Ananiev, E.V. Simmons, C.R. (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol. 146, 250 264.
13. Dickmann, D.I., Isebrands, J.G., Blake, T.J., Kosola, K. Kort, J. (2001) Physiology ecology of poplars. In Poplar Culture in North America, Part 2 (Dickmann, D.I., Isebrands, J.G., Eckenwalder, J.E. Richardson, J. eds).
14. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792 1797.
15. Falusi, M. Calamassi, R. (1990) Bud dormancy in beech (Fagus sylvatica L.). Effect of chilling and photoperiod on dormancy release of beech seedlings. Tree Physiol. 6, 429 438.
16. Filichkin, S.A., Meilan, R., Busov, V.B., Ma, C., Brunner, A.M. Strauss, S.H. (2006) Alcohol-inducible gene expression in transgenic Populus. Plant Cell Rep. 25, 660 667.
17. Foucher, F., Morin, J., Courtiade, J., Cadioux, S., Ellis, N., Banfield, M.J. Rameau, C. (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell, 15, 2742 2754.
18. Gleave, A.P. (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20, 1203 1207.
19. Grbic, V. Bleecker, A.B. (2000) Axillary meristem development in Arabidopsis thaliana. Plant J. 21, 215 223.
20. Greenwood, M.S. (1995) Juvenility and maturation in conifers: current concepts. Tree Physiol. 15, 433 438.
21. Gutierrez, L., Van Wuytswinkel, O., Castelain, M. Bellini, C. (2007) Combined networks regulating seed maturation. Trends Plant Sci. 12, 294 300.
22. Gutierrez, L., Mauriat, M., Guenin, S. et al. (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnol. J. 6, 609 618.
23. Hedman, H., Kallman, T. Lagercrantz, U. (2009) Early evolution of the MFT-like gene family in plants. Plant Mol. Biol. 70, 359 369.
24. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. Vandesompele, J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
25. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S. Mullineaux, P.M. (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819 832.
26. Helliwell, C.A., Wood, C.C., Robertson, M., Peacock, W.J. Dennis, E.S. (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J. 46, 183 192.
27. Hepworth, S.R., Valverde, F., Ravenscroft, D., Mouradov, A. Coupland, G. (2002) Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO J. 21, 4327 4337.
28. Horvath, D.P., Anderson, J.V., Chao, W.S. Foley, M.E. (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci. 8, 534 540.
29. Howe, G.T., Aitken, S.N., Neale, D.B., Jermstad, K.D., Wheeler, N.C. Chen, T.H.H. (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can. J. Bot. 81, 1247 1266.
30. Hsu, C.Y., Liu, Y., Luthe, D.S. Yuceer, C. (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell, 18, 1846 1861.
31. Igasaki, T., Watanabe, Y., Nishiguchi, M. Kotoda, N. (2008) The FLOWERING LOCUS T/TERMINAL FLOWER 1 family in Lombardy poplar. Plant Cell Physiol. 49, 291 300.
32. Kalluri, U.C., Difazio, S.P., Brunner, A.M. Tuskan, G.A. (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol. 7, 59.
33. Kardailsky, I., Shukla, V.K., Ahn, J.H., Dagenais, N., Christensen, S.K., Nguyen, J.T., Chory, J., Harrison, M.J. Weigel, D. (1999) Activation tagging of the floral inducer FT. Science, 286, 1962 1965.
34. Kobayashi, Y. Weigel, D. (2007) Move on up, it's time for change - mobile signals controlling photoperiod-dependent flowering. Genes Dev. 21, 2371 2384.
35. Kobayashi, Y., Kaya, H., Goto, K., Iwabuchi, M. Araki, T. (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science, 286, 1960 1962.
36. Kotoda, N., Iwanami, H., Takahashi, S. Abe, K. (2006) Antisense Expression of MdTFL1, a TFL1-like Gene, Reduces the Juvenile Phase in Apple. J. Amer. Soc. Hort. Sci. 131, 74 81.
37. Kumar, S., Tamura, K. Nei, M. (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 5, 150 163.
38. Li, D., Liu, C., Shen, L., Wu, Y., Chen, H., Robertson, M., Helliwell, C.A., Ito, T., Meyerowitz, E. Yu, H. (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell, 15, 110 120.
39. Liljegren, S.J., Gustafson-Brown, C., Pinyopich, A., Ditta, G.S. Yanofsky, M.F. (1999) Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell, 11, 1007 1018.
40. Livak, K.J. Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402 408.
41. Long, J. Barton, M.K. (2000) Initiation of axillary and floral meristems in Arabidopsis. Dev. Biol. 218, 341 353.
42. McSteen, P. Leyser, O. (2005) Shoot branching. Annu. Rev. Plant. Biol. 56, 353 374.
43. Michaels, S.D., Himelblau, E., Kim, S.Y., Schomburg, F.M. Amasino, R.M. (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiol. 137, 149 156.
44. Mimida, N., Goto, K., Kobayashi, Y., Araki, T., Ahn, J.H., Weigel, D., Murata, M., Motoyoshi, F. Sakamoto, W. (2001) Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells, 6, 327 336.
45. Mohamed, R. (2006) Expression and Function of Populus Homologs to TERMINAL FLOWER1 Genes: Roles in Onset of Flowering and Shoot Phenology.
46. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
47. Pnueli, L., Carmel-Goren, L., Hareven, D., Gutfinger, T., Alvarez, J., Ganal, M., Zamir, D. Lifschitz, E. (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development, 125, 1979 1989.
48. Pnueli, L., Gutfinger, T., Hareven, D., Ben-Naim, O., Ron, N., Adir, N. Lifschitz, E. (2001) Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell, 13, 2687 2702.
49. Ratcliffe, O.J., Amaya, I., Vincent, C.A., Rothstein, S., Carpenter, R., Coen, E.S. Bradley, D.J. (1998) A common mechanism controls the life cycle and architecture of plants. Development, 125, 1609 1615.
50. Ratcliffe, O.J., Bradley, D.J. Coen, E.S. (1999) Separation of shoot and floral identity in Arabidopsis. Development, 126, 1109 1120.
51. Rinne, P.L., Kaikuranta, P.M. van der Schoot, C. (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy. Plant J. 26, 249 264.
52. Rohde, A. Bhalerao, R.P. (2007) Plant dormancy in the perennial context. Trends Plant Sci. 12, 217 223.
53. Rohde, A., Prinsen, E., De Rycke, R., Engler, G., Van Montagu, M. Boerjan, W. (2002) PtABI3 impinges on the growth and differentiation of embryonic leaves during bud set in poplar. Plant Cell, 14, 1885 1901.
54. Rohde, A., Ruttink, T., Hostyn, V., Sterck, L., Van Driessche, K. Boerjan, W. (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J. Exp. Bot. 58, 4047 4060.
55. Rottmann, W.H., Meilan, R., Sheppard, L.A., Brunner, A.M., Skinner, J.S., Ma, C., Cheng, S., Jouanin, L., Pilate, G. Strauss, S.H. (2000) Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J. 22, 235 245.
56. Ruonala, R., Rinne, P.L., Kangasjarvi, J. van der Schoot, C. (2008) CENL1 expression in the rib meristem affects stem elongation and the transition to dormancy in Populus. Plant Cell, 20, 59 74.
57. Ruttink, T., Arend, M., Morreel, K., Storme, V., Rombauts, S., Fromm, J., Bhalerao, R.P., Boerjan, W. Rohde, A. (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell, 19, 2370 2390.
58. Samach, A., Onouchi, H., Gold, S.E., Ditta, G.S., Schwarz-Sommer, Z., Yanofsky, M.F. Coupland, G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613 1616.
59. Shalit, A., Rozman, A., Goldshmidt, A., Alvarez, J.P., Bowman, J.L., Eshed, Y. Lifschitz, E. (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc. Natl Acad. Sci. USA, 106, 8392 8397.
60. Shannon, S. Meeks-Wagner, D.R. (1991) A Mutation in the Arabidopsis TFL1 Gene Affects Inflorescence Meristem Development. Plant Cell, 3, 877 892.
61. Singer, S., Sollinger, J., Maki, S., Fishbach, J., Short, B., Reinke, C., Fick, J., Cox, L., McCall, A. Mullen, H. (1999) Inflorescence architecture: a developmental genetics approach. Bot. Rev. 65, 385 410.
62. Sohn, E.J., Rojas-Pierce, M., Pan, S., Carter, C., Serrano-Mislata, A., Madueno, F., Rojo, E., Surpin, M. Raikhel, N.V. (2007) The shoot meristem identity gene TFL1 is involved in flower development and trafficking to the protein storage vacuole. Proc. Natl Acad. Sci. USA, 104, 18801 18806.
63. Sung, S. Amasino, R.M. (2005) Remembering winter: toward a molecular understanding of vernalization. Annu. Rev. Plant Biol. 56, 491 508.
64. Suzuki, M. (2003) Size structure of current-year shoots in mature crowns. Ann. Bot. (Lond.), 92, 339 347.
65. Weigel, D. Nilsson, O. (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature, 377, 495 500.
66. Welling, A. Palva, E.T. (2006) Molecular control of cold acclimation in trees. Physiol. Plant. 127, 167 181.
67. Wesley, S.V., Helliwell, C.A., Smith, N.A. et al. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581 590.
68. Wigge, P.A., Kim, M.C., Jaeger, K.E., Busch, W., Schmid, M., Lohmann, J.U. Weigel, D. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309, 1056 1059.
69. Yoo, S.Y., Kardailsky, I., Lee, J.S., Weigel, D. Ahn, J.H. (2004) Acceleration of flowering by overexpression of MFT (MOTHER OF FT AND TFL1). Mol. Cells, 17, 95 101.
70. Yuceer, C., Land, S.B., Kubiske, M.E. Harkess, R.L. (2003) Shoot morphogenesis associated with flowering in Populus deltoides (Salicaceae). Am. J. Bot. 90, 196 206.